Silva Santos et al. Journal of Ethnobiology and Ethnomedicine (2019) 15:33 https://doi.org/10.1186/s13002-019-0313-4

RESEARCH Open Access Use of in a semi-arid region of : an approach to the use value and data analysis for conservation Suellen da Silva Santos1,2,3*, Reinaldo Farias Paiva de Lucena4 , Hyago Keslley de Lucena Soares1,2,3, Vanessa Moura dos Santos Soares1,2, Natalice Santos Sales2,5 and Lívia Emanuelle Tavares Mendonça1,2,6

Abstract Background: This study aimed to survey the knowledge and use of mammals by the residents of the rural community of Capivara in the municipality of Solânea (Paraíba State, Northeast Brazil) and to propose a new method of using the use value as a tool for data analysis in ethnozoological surveys. Methods: The uses attributed to mammals were recorded through semi-structured interviews conducted with the breadwinners (men and women) living in the community. The were identified through guided tours, by descriptions made by the interviewees, and using specimens donated by them, as well as by comparison with the pertinent scientific literature (morphological and ecological). Through the use value differentiated analysis, it was possible to distinguish the current use value of the species (effective use) from their potential use value (knowledge, but no effective use) to determine their real importance related to the uses cited by the studied group. Results: Nineteen species were cited; however, only 17 of them were identified and then distributed in 13 families. The other species were identified at the genus level Leopardus sp. and order Rodentia. The species were classified into 6 categories of use: food, captive breeding, zootherapeutic, artisanal, magic/religious, and veterinary purposes. Conclusions: This article discusses possible conservation solutions, given the irregular exploitation of some species, warning about the biodiversity, and traditional knowledge conservation. Keywords: use, Ethnomastozoology, Use value, Current use value

Background have been used for food, pets, medicinal, magic/religious, The biological diversity of mammals in Brazil, described artisanal, veterinary (folk medicine used in ), and by Paglia et al. [1], comprises 701 species distributed in control (slaughter of wild animals that feed on domestic 243 genera, 50 families, and 12 orders. In the semi-arid species) purposes (e.g., [14–19]). Animals that have utility region, Albuquerque et al. [2] recorded 156 species oc- value for the population are mostly killed in hunting activ- curring in the Caatinga. This biome has gotten the at- ities, which, according to Chiarello et al. [20], represent one tention of researchers focusing on studies, with of the greatest threats to wild mammals. Consequently, this some specific surveys aimed at obtaining data on the activity has caused a significant decline in several species’ richness, ecology, ethology, physiology, distribution, and populations throughout the world [21–25], intensifying the of species (e.g., [3–9]). process of fauna extinction. Regarding the traditional use of mammals, a growing In order to understand the dynamics of use of the local number of studies have been carried out in Brazil (e.g., fauna by the populations, data collection techniques have [10–13]). In the Caatinga biome, some species of mammals been diffused and currently used by different researchers. Among these techniques, the use value index (UV) stands out as a quantitative method, proposed by Phillips and * Correspondence: [email protected] 1Universidade Federal da Paraíba, João Pessoa, Brazil Gentry [26, 27], in ethnobotanical studies, and adapted by 2UEPB, Campina Grande, Brazil Rossato et al. [28]. This method makes it possible to test Full list of author information is available at the end of the article

© The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Silva Santos et al. Journal of Ethnobiology and Ethnomedicine (2019) 15:33 Page 2 of 14

hypotheses in ethnobiological research, measuring the im- that the biomass is a determinant factor in the choice and portance of each species at the local and regional level, ac- use of wild mammals by traditional/local populations. cording to the interviewees. Thus, the following hypotheses were tested: (1) The higher The UV is used in several ethnobotanical studies (e.g., the biomass of a species, the higher its use value and (2) [29–32]) and, currently, also in ethnozoological research the calculation of the differentiated use value modifies the (e.g., [33–36]) to analyze the relative importance of a given list of the locally most important species. species. However, because it does not distinguish current use (effective use) from potential use (knowledge, but no Materials and methods effective use), this index has limitations, evidenced in Study area some ethnobotanical studies [29–31, 37]. According to La This study was carried out in the rural community of Torre-Cuadros and Islebe [29], a plant, for example, can Capivara, municipality of Solânea (latitude 06° 45′ 18″ S receive many citations of use without being currently used longitude 35° 32′ 24″ W), inserted in the geoenviron- in the analyzed population. Stagegaard et al. [38]also mental unit of the “Borborema” Plateau, located in the show that the UV is fragile since it assesses a high number “Agreste” Mesoregion and in the Solânea Microregion, of potential uses, considering that the species under this in the semi-arid region of Paraíba State, Northeast perspective have no effective use. Brazil, at 99.3 km from João Pessoa, the state capital, Therefore, Lucena et al. [39] proposed, in their studies and can be accessed via Highways BR 230/BR 041/PB in the Brazilian semi-arid region, a change in this index 105 [53] (Fig. 1). This municipality has a population of and developed the current use value (UV ), based on current 26,925 inhabitants distributed in an area of 232,096 km2; the uses that people reported as effective (currently exe- 7361 of them live in rural areas (3699 women and 3662 cuted by them), the potential use value (UV ), based potential men), and about 17,273 are literate [54]. on the uses that people stated to know, but are not cur- rently executed by them, and the general use value (UVgen- eral), commonly used in the literature and does not Data collection distinguish between effective use and knowledge. This research was carried out in 2012, through several visits Currently, many studies involving local populations to the community for data collection and other observa- [10, 40–43] have shown that mammals are the main tions. All the residences of the chosen sample were visited, sources of protein in the tropical regions of the world, but not all the family breadwinners were found, even after and this is the main factor that promotes the capture repeated visits to their residences. Therefore, 108 infor- and slaughter of these animals. Thus, the preference of mants were interviewed (52 men and 56 women). human populations for large- and medium-sized species Information on the use of mammals in the region was was also analyzed based on the Optimal Foraging The- obtained through semi-structured questionnaires, com- ory, which is a model of evolutionary ecology that has plemented by free interviews and informal conversations been used in the analysis of subsistence of human popu- [55]. The participants’ socioeconomic data were also re- lations in several studies [44, 45]. This theory predicts corded during the interviews (Table 1). that the animal will try to maximize the amount of re- Before each interview, the participants were explained source obtained (benefit) per unit of time spent on for- about the aims of the study and then were asked to sign the aging (cost) [46, 47]. informed consent form, which is required by the National However, some studies [40, 48–50] have shown that Health Council through the Ethics Research Committee when there is a lack of preferred species, hunters have to (Resolution 466/12) and approved by the State University capture a higher number of prey of less appreciated spe- of Paraíba (protocol No. 45051115.5.0000.5187). The inter- cies, as well as to increase the invested time and cover a views dealt both with the population’s socioeconomic status larger area to capture the animals. It is noteworthy that and information on the mammals in the region such as the several cultural factors (taboos involving the choice of purposes for which they are used, their respective parts species and/or hunting areas, and forms of use) are in- used, animal capture techniques, and morphological and volved in the selection, capture, and use of species by ecological descriptions of the species. local populations and have considerable impacts on the In an attempt to obtain reliable answers from the in- populations of the species used [41–43, 48, 51]. In this terviewees, a friendly dialogue was held at the first con- sense, the understanding of these factors is essential to tact with the participants, dealing with topics such as subsidize actions aimed at the management and conser- the pleasure of contact with nature, the taste of wild ani- vation of the animals used [41, 43, 52]. mal meat, and the experience transmitted through gen- Thereby, this study recorded and evaluated how wild erations. As the informal conversation was held in a mammals are used by residents of a rural community in a relaxed manner, the questions from the semi-structured semi-arid region of northeastern Brazil. It was assumed questionnaire were asked. In addition, there was more Silva Santos et al. Journal of Ethnobiology and Ethnomedicine (2019) 15:33 Page 3 of 14

Fig. 1 Map of the municipality of Solânea, state of Paraíba, northeastern Brazil. (Map: Natan Medeiros Guerra, 2014)

than one contact with the residents to strengthen the studies previously performed in the study mesore- bonds of trust between researcher and informant. gion [12, 13, 16, 57]. Guided tours were conducted during the informants’ daily activities and non-participant observation was car- Data analysis ried out [56] for a more precise recording of the animal The UV was applied to quantify the local importance of a capture techniques, the preference for species, and other species according to the interviewees [28]. In the present relevant information. study, this index was calculated based on Lucena et al. [39], To mitigate the possible effects of the non-recording considering three types of data: uses that people cited as ef- or non-veracity of information, the synchronous con- fective (known and currently applied by them) (UVcurrent), firmation of the information was made, checking the uses that people were aware of but do not themselves use data obtained from one informant with those obtained (UVpotential), and the general use value (UVgeneral)referred from others. to uses that were commonly reported in the literature but The species vernacular names were recorded exactly with no distinction between use and knowledge [28]. This as mentioned by the interviewees, and the species were distinction was made during interviews by asking the inter- identified as follows: (1) analysis of the specimens or viewees to indicate uses that were effective (current) or not their parts donated by the informants, (2) analysis of an- (potential). These values were calculated using the Micro- imals pictures taken during the interviews and during soft Excel software (2012). the monitoring of hunting activities, (3) based on ver- nacular names, with the help from taxonomists who UVcurrent ¼ Uicurrent=n knew the fauna of the study (researchers from the Fed- eral University of Paraíba - Campus I - Mastozool- where UVcurrent = current use value of the species, ogy Laboratory), and (4) based on ethnozoological Ui = number of citations of current use of the Silva Santos et al. Journal of Ethnobiology and Ethnomedicine (2019) 15:33 Page 4 of 14

Table 1 Socioeconomic profile of the respondents to treat uterine problems, bone inflammation, throat in- Gender flammation, and toothache, four different citations of Men 52 use are counted. If from this same specimen, another Women 56 biological part is used for other therapeutic indications, more uses are attributed to it. Age group With regard to the artisanal use, the citations were – 19 30 16 counted according to the specimen’s biological part used 31–50 42 (e.g., leather, carapace) and to the purposes attributed to 51–70 34 it, such as for tambourines, zabumba, saddle, chair seat, >70 1 sandal sole, seats for motorcycles, and belts, which are Not informed 15 different items representing a citation each. This logis- tics is used as a model for the other categories of use, Residency time except for breeding and control since there is no diver- > 60 years 2 sity in their description. 31–60 years 14 The one-way ANOVA was used to identify significant 15–30 years 51 differences between the results from the three types of < 15 years 35 use value calculated for each species, and the Tukey test Not informed 6 was applied to identify which means were statistically different between each other (p < 0.05 and p < 0.01). Schooling level The data analysis was performed in the Past 2.17c. Fur- Semi-illiterate 16 thermore, the similarity analysis (cluster) was performed Illiterate 34 to analyze the similarity between these UVs, using the Incomplete primary education 35 PRIMER 6.0 software. Complete primary education 4 To test if the biomass of the species predicted the use Incomplete secondary education 2 value attributed to them, a simple linear regression was made, adopting the UV as a dependent variable Complete secondary education 2 current and the biomass of each species as an independent vari- Not informed 15 able, using the BioEstat 5.0 software. Biomass was calculated by multiplying the number of species mentioned by each informant, n =total captured animals by the medium body mass of the spe- number of informants. cies, found in the literature on mammals [58–60]. ¼ Uvpotential Uipotential=n Results The interviewed residents cited 19 specimens; 17 of where UV = potential use value of the species, Ui potential them were identified at the species level and distributed = number of citations of potential use of the species men- in 13 families, the others were identified at the genus tioned by each informant, n = total number of informants. level Leopardus sp. and order Rodentia. Several kinds of use were attributed to the species, Uvgeneral ¼ Uigeneral=n which were distributed in 6 categories: food (19 species), where UVgeneral = general use value of the species, Ui = breeding (12 species), artisanal (11 species), zoothera- number of citations of general use of the species men- peutic (9 species), magic/religious (1 species), and veter- tioned by each informant, n = total number of informants. inary purposes (1 species) (Table 2). The counting of the animal species citations was made It was noticed that the informants (men and women) considering information such as preparation methods, are involved in pre- and post-hunting activities and that therapeutic indications, and artisanal purposes, and for the men are responsible for obtaining the resources by each different kind of use of the same species, an add- hunting, making products used in popular veterinary itional citation was counted. and for magic/religious purposes (popular belief). The For example, regarding food category, the citations for women are in charge of making food and zootherapeutic the use of cooked or roast meat were counted as distinct products. However, both men and women are involved uses, i.e., cooked meat was considered one kind of use in activities relating to the breeding of wild species. and roast meat another (a citation for each one). As for spixii (Wagler, 1831) (226 citations), Puma the medicinal animals, the citations were related to the yagouaroundi (É. Geoffroy Saint-Hilaire, 1803) (190 cita- specimen’s parts used and to the diseases treated by tions) and Leopardus sp. (182 citations) had the highest their uses. Therefore, when the melted animal fat is used number of citations. Regarding the utility value, G. spixii Silva Santos et al. Journal of Ethnobiology and Ethnomedicine (2019) 15:33 Page 5 of 14

Table 2 Ordering of the ten most important local species, based on the use value (UV), in the rural community of Capivara in the municipality of Solânea (Paraíba State, northeastern Brazil)

Scientific name Vernacular name UVgeneral UVcurrent UVpotential Primates Cebidae Callithrix jacchus (Linnaeus, 1758) Common marmoset ––10° Carnivora Canidae Cerdocyon thous (Linnaeus, 1766) Fox 4° 9° 3° Felidae Leopardus sp. ‘Polka dot cat’ / Wild cat’ 3° 8° 2° Puma yagouaroundi (É. Geoffroy Saint-Hilaire, 1803) Jaguarundi (Red Cat / Black Cat / Blue Cat) 2° 9° 1° Mephitidae Conepatus semistriatus (Boddaert, 1785) Skunk 7° 4° 5° Cingulata Dasypodidae Euphractus sexcinctus (Linnaeus, 1758) Yellow armadillo 7° 5° 4° Rodentia Galea spixii (Wagler, 1831) Prea 1° 1° 5° rupestris (Wied-Neuwied, 1820) Rock cavy 6° 3° 6° laurentius (Thomas, 1904) Punaré rat 5° 2° 9° Lagomorpha Leporidae Sylvilagus brasiliensis (Linnaeus, 1758) Forest rabbit 10° 10° – Pilosa Myrmecophagidae Tamandua tetradactyla (Linnaeus, 1758) Collared anteater 9° 7° 8° Didelphimorpha Didelphidae Didelphis albiventris Lund, 1840 Brazilian opossum 8° 6° 7°

had the highest general use value (UVgeneral =2.09), calculated for the species used (F = 4.048; P < 0.02467), followed by the carnivore species P. yagouaroundi (UVgen- especially between the UVcurrent and the UVgeneral (Tukey eral = 1.76) and Leopardus sp. (UVgeneral =1.68).Thero- test P < 0.05). This pattern is observed in the similarity dents G. spixii (UVcurrent = 1.49), Thrichomys apereoides analysis, in which the UVcurrent is included in a group (Lund, 1941) (UVcurrent = 1.12), and Kerodon rupestris different from the other two types of UV (Fig. 3). (Wied-Neuwied, 1820) (UVcurrent = 0.75) had the highest The results from the regression analysis (Fig. 4) show current use (effective use) values. This high UVcurrent indi- that there is no significant relationship between the bio- cates that possibly these species have been exploited locally. mass of the consumed wild animals and the UV attrib- P. yagouaroundi (UVpotential =1.50),Leopardus sp.(UVpoten- uted to them (readjusted = 0.0723; F = 0.0558; p = 0.39). tial = 1.36), and Cerdocyon thous (Linnaeus, 1766) (UVpoten- tial = 1.36) were the most prominent species regarding the Discussion potential use value (Tables 2 and 3)(Fig.2). The use of mammal species is a practice carried out all Some of the cited species are used for more than one pur- over the world [43, 61–66], demonstrating that the use pose, such as C. Thous, which was related to 6 different kinds of wild animals is supposed to be culturally dissemi- of use, especially in the local folk medicine, being used to treat nated. In the semi-arid region of Brazil, these relation- 18 pathologies (Table 3), reflecting thus its local importance. ships between humans and nature become even more According to the one-way ANOVA, there was a sig- important, because the environmental factors associated nificant difference between the three types of use value with precarious socioeconomic conditions led these Table 3 Ordering of species of local importance, based on their use value (current, potential and general), their respective use categories (Fo food, Cb captive breeding, Mag/Rel Santos Silva magic/religious, Zoot zootherapeutic, Art artisanal, Vet veterinary), zootherapeutic uses (used parts and treated diseases), and number of citations attributed to greater perceived abundance described by the residents of the rural community of Capivara, in the municipality of Solânea (Paraíba State, northeastern Brazil)

Scientific name Vernacular name Purpose UVgeneral UVpotential UVcurrent Used part Treated disease Perceived Ethnomedicine and Ethnobiology of Journal al. et abundance Primates Cebidae Callithrix jacchus (Linnaeus, 1758) Common marmoset Fo; Cb 0.22 0.18 0.04 –– 20 Carnivora Canidae Cerdocyon thous (Linnaeus, 1766) Fox Fo; Cb; Mag/Rel; Zoot; 1.42 1.16 0.26 Fat (2, 5) Uterine problems 53 Art; Vet Leather (1) Hemorrhoids Liver (7) Bone inflammation Gastritis Ulcer Throat inflammation Toothache Hemorrhage

Rheumatism (2019)15:33 General pains Asthma Infection The Flu Low uterus Infertility Pregnancy problems Cancer Worms Felidae Leopardus pardalis (Linnaeus, 1758) Ocelot Fo; Art 0.04 0.04 0 –– – Leopardus spp. “Polka dot cat”/“Wild cat” Fo; Cb; Zoot; Art 1.68 1.36 0.32 Leather (1) Inflammation 20 Puma concolor (Linnaeus, 1771) Puma Fo; Art 0.04 0.04 0 –– – Puma yagouaroundi (É. Geoffroy Saint- Jaguarundi (Red Cat/Black Cat/ Fo; Cb; Zoot; Art 1.76 1.50 0.26 Leather (1) Inflammation 26 Hilaire, 1803) Blue Cat) Mephitidae Conepatus semistriatus (Boddaert, 1785) Skunk Fo; Zoot 1.10 0.60 0.50 Bones (7, 4) Back pain 25 Meat (8) Rheumatism Liver (6) Diabetes Mustelidae

Galitictis cuja (Molina, 1782) Lesser grison Fo; Cb; Art 0.10 0.08 0.03 –– 13 14 of 6 Page Procyonidae Procyon cancrivorous Storr,1780 Crab-eating raccoon Fo; Art 0.13 0.13 0 –– 21 Rodentia —Rat / ‘Fava bean rat’ Fo 0.03 0.02 0.01 –– 10 Table 3 Ordering of species of local importance, based on their use value (current, potential and general), their respective use categories (Fo food, Cb captive breeding, Mag/Rel Santos Silva magic/religious, Zoot zootherapeutic, Art artisanal, Vet veterinary), zootherapeutic uses (used parts and treated diseases), and number of citations attributed to greater perceived abundance described by the residents of the rural community of Capivara, in the municipality of Solânea (Paraíba State, northeastern Brazil) (Continued)

Scientific name Vernacular name Purpose UVgeneral UVpotential UVcurrent Used part Treated disease Perceived Ethnomedicine and Ethnobiology of Journal al. et abundance Caviidae Kerodon rupestris (Wied-Neuwied, 1820) Rock cavy Fo; Cb; Zoot; Art 1.19 0.44 0.75 Fat (2) For eye cleansing 12 Meat (3) Weakness Intestine (4) Shortness of breath Skin (4) Foot leather (4) Galea spixii (Wagler, 1831) Prea Fo; Cb; Zoot 2.09 0.60 1.49 Bones (6) Mumps 39 Fat (5) Rheumatism Head (3) For teeth strengthening Cuniculidae Cuniculus paca (Linnaeus, 1766) Paca Fo 0.02 0.02 0 –– –

Echimyidae (2019)15:33 Thrichomys laurentius (Thomas, 1904) Punaré rat Fo; Cb 1.38 0.26 1.12 –– 25 Lagomorpha Leporidae Sylvilagus brasiliensis (Linnaeus, 1758) Forest rabbit Fo; Cb 0.29 0.12 0.18 –– 5 Cingulata Dasypodidae Dasypus novemcinctus (Linnaeus, 1758) Armadillo Fo; Cb; Zoot 0.22 0.06 0.16 Fat (5) Throat inflammation 3 Cough Euphractus sexcinctus (Linnaeus, 1758) Yellow armadillo Fo; Cb; Zoot; Art 1.10 0.65 0.45 Fat (5) Throat inflammation 12 Cough Didelphimorpha Didelphidae Didelphis albiventris Lund, 1840 Brazilian opossum Fo; Art 0.86 0.43 0.42 –– 24 Pilosa Myrmecophagidae Tamandua tetradactyla (Linnaeus, 1758) Collared anteater Fo; Cb; Zoot; Art 0.63 0.30 0.33 Intestine (7) Back pain 6 Skin (7) General pains

Nail (7) Asthma 14 of 7 Page Fat (7) Method of use for the treatment of diseases: (1) After tanning the leather, you sit on it; (2) melt and drip it on the hurt area; (3) cook it and drink the broth; (4) toast, macerate it, and make a tea; (5) melt and drink with coffee or pure; (6) toast, macerate, and ingest the powder; (7) toast, macerate, and mix with food or drink; (8) eat the meat Silva Santos et al. Journal of Ethnobiology and Ethnomedicine (2019) 15:33 Page 8 of 14

Fig. 2 Photographic records of species cited by the residents of the rural community of Capivara in the municipality of Solânea (Paraíba State, northeastern Brazil) people to develop a very unique sociocultural structure natural resources, depending on the study region. The and a strong relationship with the faunistic and floristic data obtained in our study indicate that men and women resources of their region. This is reported in several stud- know and use the same species. Concerning the mas- ies (e.g., [16, 67–71]), especially during drought periods, tery of the categories, men, because they are mostly when the agriculture and the raising of domestic animals in contact with nature, work outside the residences, are not feasible due to the lack of resources [16, 42]. and besides performing cinegetic activities, they are Lucena et al. [72] explain that men and women have more related to these practices. However, women different patterns of knowledge (similar or not) of the demonstrate mastery in preparing the animals used

Fig. 3 Similarity analysis between the UVcurrent,UVgeneral, and UVpotential of mammal species used in the rural community of Capivara, in the municipality of Solânea (Paraíba State, northeastern Brazil). Gray triangle: UVcurrent. Black inverted triangle: UVgeneral. Gray square: UVpotential. Silva Santos et al. Journal of Ethnobiology and Ethnomedicine (2019) 15:33 Page 9 of 14

In addition to the leather, an informant described the use of hoof of Euphractus sexcinctus (Linnaeus, 1758) to decorate the residence. Another interviewee reported the use of rennet (stomach) of K. rupestris in the prepar- ation of cheese, making the process faster; this trend has already been recorded in other research [78]. The species related to the traditional medicinal use corroborate the list of mammals described by re- searchers over the years in Brazil [10, 12, 36, 70, 78]. With regard to the magic/religious and veterinary cat- egories, C. thous had one citation in each one of them. For the first purpose, the tail is placed on domestic ani- mals (cattle, goats, and sheep) to prevent the approach of bat species. For the traditional veterinary practice, “lard” (animal fat) is melted and then applied to fe- males of domestic animals, such as cows, goats, and

Fig. 4 Relationship between the biomass and the UVcurrent of the sheep, after the delivery process in order to clean the species used in the rural community of Capivara, in the municipality uterus of these animals. of Solânea (Paraíba State, northeastern of Brazil) Thus, utility citations relating to the species reflect their general use value, which may or may not be al- in the culinary and those related to folk medicinal tered when the analysis of the current use value is treatments. This can be explained by the fact that performed. It should be noted that the low current women are usually responsible for domestic activities use value may be related to several factors, such as a and family welfare. reduction in the use and concealment of information, All the species described were attributed to food pur- due to the illegal use of wild animals. pose, obtaining a higher number of citations and higher Another factor possibly related to this preference, use values; these animals are important because they are based on the interviews, is justified by two biases: (1) much appreciated in the local cuisine. This trend of Perceived abundance of these animals, since, when the preference for some animal species as a food resource informants were asked about the abundance of species, has already been observed in some studies in the world C. thous and G. spixii was described as one of the most [16, 42, 66, 73–77] and also in the studied community, found in the region (respectively, 53 and 39 citations re- where the hunting is directed to animals of which meat ferring to high abundance perceived). This data was col- is considered tasty. lected through visual stimulation, using figures (squares) Regarding the breeding category, some studies show containing different numbers of dots to represent the that this relationship between human populations and ani- perceived abundance of the species in the area, seeking mals is common in the semi-arid region of Brazil [12, 24, to standardize and reduce the subjectivity of the infor- 78]. In the study area, the species are used as pets due to mation provided by the interviewees. the affective bond and their beauty (e.g., Leopardus sp.) (2) Spatial distribution, all the informants (n = 108) in- and because they can later be used as food resource (e.g., dicated the different areas where the mentioned species Euphractus sexcinctus)(Fig.2), reflecting their number of may be found, extending from conserved areas to citations. The latter one (food resource) is also reported anthropized areas, since G. spixii is found in several en- by Alves et al. [78]. vironments distinguishable by the informants, such as The carnivorous species had a significant number of ci- open field, closed field, quarries, crops of forage cactus, tations for artisanal purposes, and leather was commonly and near the residences, which reflected its high number cited as the material used to make musical items, such as of citations and higher general use value and current use tambourine and zabumba, as well as saddles, motorcycle value. Some studies conducted in traditional communi- seats, chair covers, car seats, shoe and boot soles, bags, ties also reported the identification of ecological zones hats, key rings, and belts, among others. However, none of by the informants (e.g., [79, 80]). Such specialties relat- these ornaments were seen in the visited residences. Thus, ing to local ecological knowledge facilitate the collection the UVgeneral attributed by the interviewees to the species of specimens (animals), making possible the attribution for ornamental purposes, evidences their local importance, of utility value to the animals. even though they are not currently used. Nevertheless, 11 Some of the cited species are used for more than one respondents reported executing the use (UVcurrent)ifthe purpose. The multiple uses of a species can be discussed animals are slaughtered. from two different points of view. The former is a Silva Santos et al. Journal of Ethnobiology and Ethnomedicine (2019) 15:33 Page 10 of 14

conservationist because the use of a species for different (Linnaeus, 1758) (1–5 kg) had high UVgeneral and UVcur- purposes means additional uses or hunting and may re- rent (Table 3) and high reproductive and density rates, sult in pressure on this species. The more diversified the and except for Kerodon rupestris (WIED-NEUWIED, attributions to a species are, the higher the chance of it 1820), all these species are generalist as for the use of being known/used by the population and the higher habitat, are widely distributed, and tolerate anthropo- probability of it being introduced into the culture by re- genic disturbances (r-strategists) [9, 97–102]. placing an extinct species [18, 24, 78, 81–83]. K. rupestris despite being a specialist in using habitats The second one concerns the optimization of the use (rocky outcrops and mountainous areas), it has a high of natural resources by the local community, considering reproductive rate and gregarious habit [9, 103]. This spe- that, due to the peculiar socioeconomic situation of the cies is endemic to the Caatinga, and although it is widely residents, they attempt to make the most of the available distributed throughout this biome, it is classified as vul- resources, since a large part of these by-products (tails, nerable on the national list of endangered species, due carapace, bones) would be discarded [18, 24, 78, 83, 84]. to the hunting pressure [104]. Thus, the same species can have its by-products used as With regard to D. novemcinctus and E. sexcinctus, ac- food, in traditional medicine, to make some items, etc. cording to Marinho et al. [105], the abundance of these Mendonça et al. [85], in a study carried out in the semi- species in areas of Caatinga is very relative and although arid region of Brazil, reported that it is quite common they are hunted in several areas [12, 16, 35, 42, 70, 78, for local hunters to make the most of the hunted animal 88, 106, 107] they are widely distributed in the biome. parts, resulting in at least two distinct uses for the ma- Other medium-sized species (1–5 kg) such as Conepatus jority of cinegetic resources, including species consid- amazonicus (Lichtenstein, 1838) and Tamandua tetra- ered dangerous to man or to domestic animals. dactyla (Linnaeus, 1758), despite having low population In the present work, the biomass of the species had no densities and low reproductive rates, are easily found in influence on their UVcurrent, evidenced in the simple lin- several areas of the Caatinga [9]. ear regression (the relationship between biomass and the Regarding C. thous, it is reported in the literature as a UVcurrent). Although according to the Optimal Foraging medium-sized animal with the highest number of re- Theory, local populations prefer to use animals of higher cords in Paraíba, Pernambuco, Ceará, and Alagoas. This biomass, obtaining a greater quantity of resources per species occurs in all habitats, visibly adaptable to anthro- hunting and/or manufacturing time [40, 46, 48], several pized areas, and is found even in green areas of cities [9, studies have reported that as the medium- and large- 108]. Thus, it is constantly seen, which results in its high sized species are depleted, typical species with higher perceived abundance, described by the interviewees, and availability become the subsequent targets [40, 42, 78, in the consequent association with purposes of use. 86–90]. In fact, this is the trend pointed out in ethnobio- With regard to the mesopredator carnivorous (5–10 logical studies around the world (e.g., [91–96]). There- kg) such as tayras (Eira barbara), crab-eating raccoon fore, small-sized species may be as important for the (Procyon cancrivorus), and all Felidae species and top communities as large-sized species (higher biomass). predators such as Puma concolor (Linnaeus, 1771) (> 15 Some authors have reported the hunting of small-sized kg), some studies have shown that these species already species in other semi-arid areas in Brazil, such as Men- occur in low population densities and have ecological donça et al. [88], who investigated the preference of and behavioral peculiarities which make them more vul- hunters for species of large, medium, and low body bio- nerable to anthropogenic pressures [9, 97, 98, 9105, 10 ]. mass and found that hunters in the semi-arid region have The felines recorded in the present study, except for no significant preference for large-sized animals. There- Leopardus pardalis (Linnaeus, 1758), are classified as fore, people have developed a peculiar way of dealing with vulnerable on the national and international lists of en- and making the most of available resources, which are dangered species [104, 110]. The state of P. concolor is often obtained in large quantities, thus making up for the more critical in the Caatinga than it is in the national low body weight of species of local importance. classification; in this biome, this species is classified as Several cultural and ecological factors are associated endangered [105, 111]. with the choice and use of species in the Caatinga [16, Another important factor is that although there are 42, 87, 88], which may justify the variations between the many large-sized animals in the Caatinga [9, 105], they are different use values attributed to each species (see Table strongly affected by hunting and habitat loss because they 3). For example, small- (< 1 kg) and medium-sized spe- are k-specialists and have several trophic requirements, cies (1–5 kg) such as G. spixii, T. apereoides, K. rupestris, low reproductive rate, long lifetime, and are very suscep- Didelphis albiventris Lund, 1840 and Callithrix jacchus tible to anthropogenic disturbances [9, 97, 98, 105]. (Linnaeus, 1758) (< 1 kg), Dasypus novemcinctus (Lin- All these factors are aggravated by the increased arid- naeus, 1758), E. sexcinctus, and Sylvilagus brasiliensis ity and increase in areas susceptible to desertification Silva Santos et al. Journal of Ethnobiology and Ethnomedicine (2019) 15:33 Page 11 of 14

since 20% of the Caatinga is undergoing desertification of the species, based on the Cluster test and one- [106, 112]. This may explain the absence of many other wayANOVA. No studies had statistically measured this species, evidencing the need for future studies aimed to difference, until now, although some authors have pointed investigate how wild populations respond to the impacts out the need to assess the applicability of this index [92, caused by human activities. It is worth mentioning that, 107, 113–115]. Therefore, the data from this research sug- in this ecosystem, most studies on the ecology of species gest a new standard for data analysis using the UVcurrent as and on factors associated with anthropogenic impacts a strategic tool for the conservation of the most important are still local and incipient [9, 16, 35, 105]. species. The systematization in data organization works as The UVcurrent of the cited species ranged from zero to a support for more reliable comparisons between ethnobi- 1.49 and the UVpotential from 0.02 to 1.57. Most of the ological studies. Thereby, the present ethnozoological animals had UVs (general, potential, and current) lower study, since its data is quantitatively interpreted, needs to than 1, but eight species had higher UVs, which reflect be categorized and delimited to provide reliable results on their local importance to the community. Thus, a high how these people use natural resources. UVcurrent is worrisome in the case of local exploitation; however, a high UVpotential may indicate the lack of spe- Conclusions cies in the region [90, 107]. It is worth noting that al- In this context, it is expected that other studies, using this though species of high potential use values are not differentiated UV method, systematize the calculation ac- effectively used, they can become part of the regular uses cording to each citation described by informants, consid- – as the currently used species are extinct [39, 90 93]. An- ering that such information may be situational and other relevant consideration is that species with high po- modifiable according to the area and time where the re- tential use may be absent in the region, which may search will be developed. However, these studies must be explain the recognition and no effective use of potential able to point out which species possibly require conserva- species [92, 107]. tion strategies to minimize negative impacts on biodiver- Although we have collected no quantitative data on sity. Such information becomes increasingly necessary not consumption frequency and number of animals slaugh- only for the preservation of the Caatinga but also for other tered, as well as no data on species abundance, fre- ecosystems in which there is a relationship between quency, and use of habitat, based on information from humans and natural resources for utilitarian purposes. local residents and other studies on hunting and use of The understanding of this technique and its consequent wild animals in the Caatinga [10, 12, 16, 42, 70, 88], the standardization proposed in this article can represent a use of wild mammals is widely disseminated in several fundamental reference for future ethnozoological studies areas and is the main cause of population reduction and and may contribute to the development of management local extinction of several species [35, 42, 101, 109]. plans and sustainable use of the wild fauna by traditional – Some studies [90, 107, 113 115] have shown that the populations that depend on this resource for survival. application of differentiated UV results in more precise diagnoses regarding the cultural importance of the spe- Acknowledgements cies used. Thereby, aiming at strategies for the conserva- The authors would like to thank all the participating locals for their warm reception and for agreeing to participate in the study. tion of these animals, further studies are needed to evaluate if the local decrease in the population of some Authors’ contributions species, from the informants’ point of view, is directly SSS, HKLS, VMSS, and NSL collected and analyzed the data and wrote the related to their use and/or to other factors, such as manuscript; LETM and RFPL coordinated the field research and the writing of the manuscript. All authors read and approved the final manuscript. population fluctuation and changes in their habitat, among others. These factors may be associated with the Funding capture/use of the species and are fundamental data for Not applicable. the development of conservation strategies. Although the UV is a data analysis tool widely used in Availability of data and materials The authors do not wish to provide data from their studies, as some recent ethnobiological studies, a standard method for col- databases charge fees and there is no proper Brazilian database. lecting and analyzing the data on the uses cited by the in- terviewees has not yet been established. This divergence Ethics approval and consent to participate in obtaining information may provide a margin for crucial The aim of this study was explained to each informant, who was then asked to sign a consent form, as required by the National Health Council and the errors in the results obtained by the researchers. Research Ethics Committee (Resolution 466/12). This research was approved The results presented here show the importance of by the Research Ethics Committee of the State University of Paraíba (Protocol No. 45051115.5.0000.5187). The authors interviewed 108 informants, adopting the UVcurrent in the analysis of ethnobiological who were informed of the aim of this scientific research and agreed to sign data since this UV explains the effective use of natural an informed consent form, according to necessary standards, and as resources and is significantly different from the UVgeneral described in the methodology through the protocol number. Silva Santos et al. Journal of Ethnobiology and Ethnomedicine (2019) 15:33 Page 12 of 14

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